Rapid, transient effects of the protein kinase C activator phorbol 12-myristate 13-acetate on activity and trafficking of the rat high-affinity choline transporter

Neuroscience

Volumn 167, Issue 3, 2010, Pages 765-773

  Black, S A G ^a,b   Ribeiro, F M ^a,b   Ferguson, S S G ^a,b   Rylett, R J ^a,b  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b WESTERN UNIVERSITY   (Canada)

Author keywords

Acetylcholine; Choline transport; Cholinergic; Phosphorylation; Protein kinase C

Indexed keywords

BISINDOLYLMALEIMIDE; CHOLINE; PHORBOL 13 ACETATE 12 MYRISTATE;

ARTICLE; BINDING AFFINITY; BINDING KINETICS; BIOTINYLATION; CELL MEMBRANE TRANSPORT; CELL SURFACE; CHOLINE UPTAKE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; ENZYME INHIBITION; HUMAN; HUMAN CELL; INTERNALIZATION; MEMBRANE COMPONENT; PRIORITY JOURNAL; PROTEIN FUNCTION; REACTION TIME; TRANSPORT KINETICS;

ACETYLCHOLINE; ANIMALS; BRAIN; CELL LINE, TUMOR; CELL MEMBRANE; ENDOCYTOSIS; ENZYME ACTIVATION; ENZYME INHIBITORS; KINETICS; MEMBRANE POTENTIALS; NERVE TISSUE PROTEINS; NEURONS; PHOSPHORYLATION; PLASMA MEMBRANE NEUROTRANSMITTER TRANSPORT PROTEINS; PROTEIN KINASE C; PROTEIN TRANSPORT; RATS; TETRADECANOYLPHORBOL ACETATE;

EID: 77951299060     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.02.026     Document Type: Article

References (43)

1. Allgaier C., Daschmann B., Huang H.Y., Hertting G. Protein kinase C and presynaptic modulation of acetylcholine release in rabbit hippocampus. Br J Pharmacol 1988, 93:525-534.
2. Apparsundaram S., Ferguson S.M., George A.L., Blakely R.D. Molecular cloning of a human hemicholinium-3-sensitive choline transporter. Biochem Biophys Res Commun 2000, 276:862-867.
3. Birks R., MacIntosh F.C. Acetylcholine metabolism of a sympathetic ganglion. Can J Biochem Physiol 1961, 39:787-827.
4. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye-binding. Anal Biochem 1976, 72:248-254.
5. Breer H., Knipper M. Regulation of high affinity choline uptake. J Neurobiol 1990, 21:269-275.
6. Cancela J.M., Bertrand N., Beley A. Involvement of cAMP in the regulation of high affinity choline uptake by rat brain synaptosomes. Biochem Biophys Res Commun 1995, 213:944-949.
7. Carrasco S., Merida I. Diacylglycerol, when simplicity becomes complex. Trends Biochem Sci 2007, 32:27-36.
8. Cooke L.J., Rylett R.J. Inhibitors of serine/threonine phosphatases increase membrane-bound choline acetyltransferase activity and enhance acetylcholine synthesis. Brain Res 1997, 751:232-238.
9. Ferguson S.M., Blakely R.D. The choline transporter resurfaces: new roles for synaptic vesicles?. Mol Interv 2004, 4:22-37.
10. Ferguson S.M., Savchenko V., Apparsundaram S., Zwick M., Wright J., Heilman C.J., Yi H., Levey A.I., Blakely R.D. Vesicular localization and activity-dependent trafficking of presynaptic choline transporters. J Neurosci 2003, 23:9697-9709.
11. Gates J., Ferguson S.M., Blakely R.D. Regulation of choline transporter surface expression and phosphorylation by protein kinase C and protein phosphatase 1/2. J Pharmacol Exp Ther 2004, 310:536-545.
12. Guermonprez L., O'Regan S., Meunier F.M., Morot-Gaudry-Talarmain Y. The neuronal choline transporter CHT1 is regulated by immunosuppressor-sensitive pathways. J Neurochem 2002, 82:874-884.
13. Guyenet P., Lefresne P., Rossier J., Beaujouan J.C., Glowinski J. Inhibition by hemicholinium-3 and antiparkinson drugs on (14C)acetylcholine synthesis and (3H)choline uptake in rat striatal synaptosomes. Mol Pharmacol 1973, 9:630-639.
14. Haga T. Synthesis and release of (14C)acetylcholine in synaptosomes. J Neurochem 1971, 18:781-798.
15. Hoffert J.D., Fenton R.A., Moeller H.B., Simons B., Tchapyjnikov D., McDill B.W., Yu M.J., Pisitkun T., Chen F., Knepper M.A. Vasopressin-stimulated increase in phosphorylation at Ser269 potentiates plasma membrane retention of aquaporin-2. J Biol Chem 2008, 283:24617-24627.
16. Ishikawa Y., Eguchi T., Ishida H. Mechanism of beta-adrenergic agonist-induced transmural transport of glucose in rat small intestine. Regulation of phosphorylation of SGLT1 controls the function. Biochim Biophys Acta 1997, 1357:306-318.
17. Issa A.M., Gauthier S., Collier B. Effects of the phosphatase inhibitors calyculin A and okadaic acid on acetylcholine synthesis and content of rat hippocampal formation. J Neurochem 1996, 66:1924-1932.
18. Ivy M.T., Newkirk R.F., Karim M.R., Mtshali C.M., Townsel J.G. Hemicholinium-3 mustard reveals two populations of cycling choline cotransporters in Limulus. Neuroscience 2001, 102:969-978.
19. Knipper M., Kahle M., Breer H. Regulation of hemicholinium binding sites in isolated nerve terminals. J Neurobiol 1992, 23:163-172.
20. Ko B., Joshi L.M., Cooke L.L., Vazquez N., Musch M.W., Hebert S.C., Gamba G., Hoover R.S. Phorbol ester stimulation of RasGRP1 regulates the sodium-chloride cotransporter by a PKC-independent pathway. Proc Natl Acad Sci U S A 2007, 104:20120-20125.
21. Leenders A.G., Sheng Z.H. Modulation of neurotransmitter release by the second messenger-activated protein kinases: implications for presynaptic plasticity. Pharmacol Ther 2005, 105:69-84.
22. Melikian H.E. Neurotransmitter transporter trafficking: endocytosis, recycling and regulation. Pharmacol Ther 2004, 104:17-27.
23. Minic J., Molgo J., Karlsson E., Krejci E. Regulation of acetylcholine release by muscarinic receptors at the mouse neuromuscular junction depends on the activity of acetylcholinesterase. Eur J Neurosci 2002, 15:439-448.
24. Nakata K., Okuda T., Misawa H. Ultrastructural localization of high-affinity choline transporter in the rat neuromuscular junction: enrichment on synaptic vesicles. Synapse 2004, 53:53-56.
25. Okuda T., Haga T. Functional characterization of the human high-affinity choline transporter. FEBS Lett 2000, 484:92-97.
26. Okuda T., Haga T., Kanai Y., Endou H., Ishihara T., Katsura I. Identification and characterization of the high-affinity choline transporter. Nat Neurosci 2000, 3:120-125.
27. Ribeiro F.M., Alves-Silva J., Volknandt W., Martins-Silva C., Mahmud H., Wilhelm A., Gomez M.V., Rylett R.J., Ferguson S.S., Prado V.F., Prado M.A. The hemicholinium-3 sensitive high affinity choline transporter is internalized by clathrin-mediated endocytosis and is present in endosomes and synaptic vesicles. J Neurochem 2003, 87:136-146.
28. Ribeiro F.M., Black S.A., Cregan S.P., Prado V.F., Prado M.A., Rylett R.J., Ferguson S.S. Constitutive high-affinity choline transporter endocytosis is determined by a carboxyl-terminal tail dileucine motif. J Neurochem 2005, 94:86-96.
29. Ribeiro F.M., Pinthong M., Black S.A., Gordon A.C., Prado V.F., Prado M.A., Rylett R.J., Ferguson S.S. Regulated recycling and plasma membrane recruitment of the high-affinity choline transporter. Eur J Neurosci 2007, 26:3437-3448.
30. Ribeiro F.M., Ferreira L.T., Marion S., Fontes S., Gomez M., Ferguson S.S., Prado M.A., Prado V.F. SEC14-like protein 1 interacts with cholinergic transporters. Neurochem Int 2007, 50:356-364.
31. Santafe M.M., Salon I., Garcia N., Lanuza M.A., Uchitel O.D., Tomas J. Modulation of ACh release by presynaptic muscarinic autoreceptors in the neuromuscular junction of the newborn and adult rat. Eur J Neurosci 2003, 17:119-127.
32. Santafe M.M., Lanuza M.A., Garcia N., Tomas J. Muscarinic autoreceptors modulate transmitter release through protein kinase C and protein kinase A in the rat motor nerve terminal. Eur J Neurosci 2006, 23:2048-2056.
33. Shapira R., Silberberg S.D., Ginsburg S., Rahamimoff R. Activation of protein kinase C augments evoked transmitter release. Nature 1987, 325:58-60.
34. Shu Y., Liu X., Yang Y., Takahashi M., Gillis K.D. Phosphorylation of SNAP-25 at Ser187 mediates enhancement of exocytosis by a phorbol ester in INS-1 cells. J Neurosci 2008, 28:21-30.
35. Simon J.R., Kuhar M.G. Impulse-flow regulation of high affinity choline uptake in brain cholinergic nerve terminals. Nature 1975, 255:162-163.
36. Veyhl M., Wagner C.A., Gorboulev V., Schmitt B.M., Lang F., Koepsell H. Downregulation of the Na(+)-d-glucose cotransporter SGLT1 by protein RS1 (RSC1A1) is dependent on dynamin and protein kinase C. J Membr Biol 2003, 196:71-81.
37. Vogelsberg V., Neff N.H., Hadjiconstantinou M. Cyclic AMP-mediated enhancement of high-affinity choline transport and acetylcholine synthesis in brain. J Neurochem 1997, 68:1062-1070.
38. Wang B., Yang L., Wang Z., Zheng H. Amyolid precursor protein mediates presynaptic localization and activity of the high-affinity choline transporter. Proc Natl Acad Sci U S A 2007, 104:14140-14145.
39. Wierda K.D., Toonen R.F., de Wit H., Brussaard A.B., Verhage M. Interdependence of PKC-dependent and PKC-independent pathways for presynaptic plasticity. Neuron 2007, 54:275-290.
40. Wright E.M., Hirsch J.R., Loo D.D., Zampighi G.A. Regulation of Na+/glucose cotransporters. J Exp Biol 1997, 200:287-293.
41. Xie J., Guo Q. Par-4 inhibits choline uptake by interacting with CHT1 and reducing its incorporation on the plasma membrane. J Biol Chem 2004, 279:28266-28275.
42. Yamamura H.I., Snyder S.H. Choline: high-affinity uptake by rat brain synaptosomes. Science 1972, 178:626-628.
43. Yamamura H.I., Snyder S.H. High-affinity transport of choline into synaptosomes of rat brain. J Neurochem 1973, 21:1355-1374.